IOC Science and Communication Centre on Harmful Algae University of Copenhagen

Harmful dinoflagellates, Prorocentrum, page 1 of 5

Module III
Section 2, Prorocentrales (2 hours)
Contents: 2.1. Suggested reading 2.2. Genus Prorocentrum Taxonomy Morphology Identification of species 2.3. Harmful species 2.4. References References in bold are available as pdf files on the course CD.

2.1. Suggested reading

Present document and the following paper: Tindall, D.R. & Morton, S.L. 1998. Community dynamics and physiology of epiphytic/benthic dinoflagellates associated with ciguatera. In: Anderson, D.M., Cembella, A.D. & Hallegraeff, G.M. (eds), Physiological ecology of harmful algal blooms, NATO ASI series, Series G, Ecological sciences, vol. 41, Springer-Verlag, Berlin, pp. 291-313.

2.2. Genus Prorocentrum

Taxonomy
The genus Prorocentrum was described by Ehrenberg with P. micans as the only species, and since then more than 70 species of Prorocentrum and Exuviaella Cienkowski 1881 have been described. Exuviaella is now considered a synonym of Prorocentrum by most authors, although recently McLachlan et al. (1997) argued convincingly for the reinstatement of Exuviella. Major taxonomic and floristic accounts include Schiller (1933), Dodge (1975), and Steidinger (1997), and for the harmful species particularly Fukuyo (1981), Faust et al. (1999), and Taylor et al. (2004). Grzebyk et al. 1998 studied the phylogenetic relationship of some species of Prorocentrum and Pearce & Hallegraeff (2004) compared freshwater/brackish species with their marine congeneric species.

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Morphology
The cells are laterally compressed, and composed of two large platelets and a number of small plates in the flagellar area (see Graham, Graham & Wilcox 2009, p. 191, fig.11-10a). The left valve is more or less flat anteriorly, whereas the right valve has an excavation into which the platelets of the flagellar pore area are fitted. Some species possess (an) apical spine(s). All known species of Prorocentrum have two chloroplasts.

Identification of species
The characters used to differentiate the species of Prorocentrum relate to the following features: cell shape and size, apical spine, pyrenoids, nucleus, and in particular surface structure and ornamentation of the valves which in some cases can be observed only by scanning electron microscopy.

2.3. Harmful species

Some planktonic species of Prorocentrum (e.g. P. micans) may form extensive blooms, but most of these bloom-forming species do not produce toxins. Cultures of P. cordatum (= P. minimum) has been shown to produce toxins in the senescent growth phase (Grzebyk et al. 1997), and blooms of this species seem to be reported still more often from around the world (Heil et al. 2005). Also the recently described planktonic species P. arabianum is toxic (Morton et al. 2002). Most harmful species of Prorocentrum are benthic or associated with substrates (Grzebyk et al. 1994, Heil et al. 1998, Tindall & Morton 1998), see also page 4. It should be noted that one of the most common benthic species reported as P. mexicanum in the recent literature has been re-investigated by Cortes-Altamirano & Sierra-Beltran (2003) who concluded that the correct name for this species is P. rhathymum while P. mexicanum is a different species clearly differentiated by the pattern formed by the valve pores. The species boundaries in Prorcentrum lima has been studied by Nagahama et al. (2011) who concluded that P. arenareum Faust 1994 is synonymous with P. lima.

2.4. References
Corts-Altamirano, R. & Sierra-Beltrn, A.P. 2003. Morphology and taxonomy of Prorocentrum mexicanum and reinstatement of Prorocentrum rhathymum (Dinophyceae). J. Phycol. 39: 221-225. Dodge, J.D. 1975. The Prorocentrales (Dinophyceae. II. Revision of the taxonomy within the genus Prorocentrum. Bot. J. Linn. Soc.71:103-125. Faust, M.A. 1990. Morphologic details of six benthic species of Prorocentrum (Pyrrophyta) from a mangrove island, Twin Cays, Belize, including two new species. J. Phycol. 26: 548-558. Faust, M. A. 1993a. Prorocentrum belizeanum, Prorocentrum elegans, Prorocentrum carribaeum, three new benthic species (Dinophyceae) from Mangrove Island, Twin Cays, Belize. J. Phycol. 29: 100-107. Faust, M. A. 1993b. Three new benthic species of Prorocentrum (Dinophyceae) from Twin Cays, Belize: P. maculosum sp. nov., P. foraminosum sp. nov., and P. formosum sp. nov. Phycologia 32: 410-418.

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Faust, M. A. 1994. Three new benthic species of Prorocentrum (Dinophyceae) from Carrie Bow Cay, Belize: P. sabulosum sp. nov, P. sculptile sp. nov., and P. arenarium sp. nov. J. Phycol. 30: 755-763. Faust, M. A. 1997. Three new benthic species of Prorocentrum (Dinophyceae) from Belize: P. norrisianum sp. nov. P. tropicalis sp. nov., and P. reticulatum sp. nov. J. Phycol. 33: 851-858. Faust, M.A., Larsen, J. & Moestrup, . 1999. Potentially toxic phytoplankton. 2. Genus Prorocentrum (Dinophyceae). ICES Identification Leaflets for Plankton, Copenhagen, International Council for the Exploration of the Sea, 12 pp. Fukuyo, Y. 1981. Taxonomical study on benthic dinoflagellates collected in coral reefs. Bulletin of the Japanese Society of Scientific Fisheries 47: 967-978. Graham, L.E. & Wilcox, L.W. 2000. Algae, Prentice-Hall Int., London. Grzebyk, D., Berland, B., Thomassin, B.A., Bosi, C. & Arnoux, A. 1994. Ecology of ciguateric dinoflagellates in the coral reef complex of Mayotte Island (S.W.Indian Ocean). J. Exp. Mar. Biol. Ecol. 178: 51-66. Grzebyk, D., Denardou, A., Berland, B. & Pouchus, Y.F. 1997. Evidence of a new toxin in the red-tide dinoflagellate Prorocentrum minimum. J. Plankton Res. 19:1111-1124. Grzebyk, D., Sako, Y., Berland, B. 1998. Phylogenetic analysis of nine species of Prorocentrum (Dinophyceae) inferred from 18S ribosomal DNA sequences, morphological comparisons and description of Prorocentrum panamensis sp. nov. J. Phycol. 34: 1055-1068. Heil, C.A., Bird, P. & Dennison, W.C. 1998. Macroalgal habitat preference of ciguatera dinoflagellates at Heron Island, A coral key in the south eastern Great Barrier Reef, Australia. In: Reguera, B., Blanco, J., Fernndez, M.L. & Wyatt, T. (eds), Harmful Algae, Proceedings of the VIII International Conference on Harmful Algae, Xunta de Galicia, Intergovernmental Oceanographic Commission of UNESCO, pp. 52-53. Heil, C. A., Glibert, P.M. & Fan, C. 2005. Prorocentrum minimum (Pavillard) Schiller. A review of a harmful algal bloom species of growing worldwide importance. Harmful Algae 4: 449-470. Hoppenrath, M. 2000. A new marine sand-dwelling Prorocentrum species, P. clipeus sp. nov. (Dinophyceae) from Helgoland, German Bight, North Sea. European Journal of Protistology 36: 29-33. Lu, D., Goebel, J., Qi, Y., Zou, J., Han, X., Gao, T. & Li, Y. 2005. Morphological and genetic study of Prorocentrum donghaiense Lu from the East China Sea, and comparison with some related Prorocentrum species, - Harmful Algae 4: 493-505. McLachlan, J.L., Boalch, G.T. & Jahn, R. 1997. Reinstatement of the genus Exuviella (Dinophyceae), Prorocentrophycidae) and an assessment of Prorocentrum lima. Phycologia 36: 38-46. Morton, S.L. 1998. Morphology and toxicology of Prorocentrum faustiae sp. nov., a new toxic species of non-planktonic dinoflagellate from Heron Island, Australia. Botanica Marina 41: 565-569. Morton, S.L., Faust, M.A., Fairey, E.I. & Moeller, P.D.R. 2002. Morphology and toxicology of Prorocentrum arabianum sp. nov. (Dinophyceae), a toxic planktonic dinoflagellate from the Gulf of Oman, Arabian Sea. Harmful Algae 1: 393-400. Nagahama, Y., Murray, S., Tomaru, A. & Fukuyo, Y. 2011. Species boundaries in the dinoflagellate Prorocentrum lima (Dinophyceae, Prorocentrales), based on morphological and phylogenetic characters. J. Phycol. 47: 178-189. Pearce, I. & G. M. Hallegraeff. 2004. Genetic affinities, ecophysiology and toxicity of Prorocentrum playfairii and P. foveolata (Dinophyceae)) from Tasmanian freshwaters. Phycologia 43 (3): 271-281.

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Puigserver, M. & Zingone, A. 2002. Prorocentrum nux sp. nov. (Dinophyceae), a small planktonic dinoflagellate from the Mediterranean Sea, and discussion of P. nanum and P. pusillum. Phycologia 41: 29-38. Schiller, J. 1933. Dinoflagellatae (Peridineae). - In: Rabenhorst, L.(ed). Kryptogamen Flora of Deutschland 10(3). I Teil. Akademische Verlagsgesellschaft, Leipzig, 617 pp. Steidinger, K.A. 1997. Dinoflagellates In: Tomas, C.R. (ed.), Identifying marine phytoplankton, Academic Press, San Diego, pp. 387-584. Taylor, F.J.R., Fukuyo, Y., Larsen, J. & Hallegraeff, G.M. 2004. Taxonomy of harmful dinoflagellates. - In: Hallegraeff, G.M., Anderson, D.M., Cembella, A.D. (eds), Manual on harmful marine microalgae, Monographs on oceanographic methodology 11, Unesco, Paris, pp. 389-432. Ten-Hage, L., Delauney, N., Pichon, V., Cout, A., Puiseux-Dao, S. & Turquet, J. 2000. Okadaic production from the marine benthic dinoflagellate Prorocentrum arenarium Faust (Dinophyceae) isolated from Europe Island coral reef ecosystem (SW Indian Ocean). Toxicon 38: 1043-1054. Ten-Hage, L., Turquet, J., Quod, J.-P., Puiseux-Dao, S. & Cout, A. 2000. Prorocentrum borbonicum sp. nov. (Dinophyceae), a new toxic benthic dinoflagellate from the southwestern Indian Ocean. Phycologia 39: 296-301. Tindall, D.R. & Morton, S.L. 1998. Community dynamics and physiology of epiphytic/ benthic dinoflagellates associated with ciguatera. In: Anderson, D.M., Cembella, A.D.& Hallegraeff, G.M. (eds), Physiological ecology of harmful algal blooms, NATO ASI series, Series G, Ecological sciences, vol. 41, Springer-Verlag, Berlin, pp. 291313. Yoo, J.S., Lee, J.H. & Fukuyo, Y. 2004. Prorocentrum vietnamensis sp. nov. (Prorocentraceae Dinophyta): a new armoured dinoflagellate from Vietnam coastal waters. J. Plant Biol. 47: 129-132.

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Prorocentrum, benthic species or species associated with substrates

Prorocentrum arabianum Morton et Faust 2002 P. arenarium Faust 1994 P. belizeanum Faust 1993 P. borbonicum Ten-Hague et al. 2000 P. carribaeum Faust 1993 P. clipeus Hoppenrath 2000 P. concavum Fukuyo 1981 P. consutum Chomerat et Nezan 2010 P. donghaiense Lu et al. 2002 P. elegans Faust 1993 P. emarginatum Fukuyo 1981 P. faustiae Morton 1998 P. foraminosum Faust 1993 P. formosum Faust 1993 P. fukuyoi Murray et Nagahama 2007 P. hoffmannianum Faust 1990 P. levis Faust, Kibler, Vandersea, Tester et Litaker 2008 P. lima (Ehrenberg) Dodge 1975 P. maculosum Faust 1993 P. mexicanum Osorio-Tafall 1942 P. norrisianum Faust 1997 P. nux Puigserver & Zingone 2002 P. panamensis Grzebyk et al. 1998 P. reticulatum Faust 1997 P. rhathymum Loeblich et al. 1979 P. ruetzlerianum Faust 1990 P. sabulosum Faust 1994 P. sculptile Faust 1994 P. tropicalis Faust 1997 P. tsawwassenense Hoppenrath et B. S. Leander 2008 P. vietnamensis Yoo et al. 2004

References
Morton et al. (2002) Faust (1994), Ten-Hage et. al. (2000) Faust (1993a), Morton et al. (1998), Faust et al. (1999) Ten-Hague et al. (2000) Faust (1993a) Hoppenrath (2000) Fukuyo (1981), Faust et al. (1999), Taylor et al. (2004) Chomerat et Nezan (2010) Lu et al. (2005) Faust (1993a) Fukuyo (1981), Faust et al. (1999), Taylor et al. (2004) Morton (1998) Faust (1993b), Faust et al. (1999) Faust (1993b) Murray & Nagahama (2007) Faust (1990), Faust et al. (1999), Taylor et al. (2004) Faust et al. (2008) Faust et al. (1999), Taylor et al. (2004) Faust (1993b), Faust et al. (1999) Cortes-Altamirano & Sierra-Beltran (2003) Faust (1997) Puigserver & Zingone (2002) Grzebyk et al. (1998) Faust (1997) Faust et al. (1999) (as P. mexicanum), Cortes-Altamirano & Sierra-Beltran (2003), Taylor et al. (2004) Faust (1990), Faust et al. (1999) Faust (1994) Faust (1994) Faust (1997) Hoppenrath & et B. S. Leander (2008) Yoo et al. (2004)